Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates

Raghav R. Poudyal, Rebecca M. Guth-Metzler, Andrew J. Veenis, Erica A. Frankel, Christine Dolan Keating, Philip C. Bevilacqua

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; however, their compatibility with essential RNA World chemistries is unclear. We show that such compartments can enhance key prebiotically-relevant RNA chemistries. We demonstrate that template-directed RNA polymerization is sensitive to polycation identity, with polydiallyldimethylammonium chloride (PDAC) outperforming poly(allylamine), poly(lysine), and poly(arginine) in polycation/RNA coacervates. Differences in RNA diffusion rates between PDAC/RNA and oligoarginine/RNA coacervates imply distinct biophysical environments. Template-directed RNA polymerization is relatively insensitive to Mg 2+ concentration when performed in PDAC/RNA coacervates as compared to buffer, even enabling partial rescue of the reaction in the absence of magnesium. Finally, we show enhanced activities of multiple nucleic acid enzymes including two ribozymes and a deoxyribozyme, underscoring the generality of this approach, in which functional nucleic acids like aptamers and ribozymes, and in some cases key cosolutes localize within the coacervate microenvironments.

Original languageEnglish (US)
Article number490
JournalNature communications
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2019

Fingerprint

Catalytic RNA
compartments
Catalysis
Polymerization
catalysis
templates
polymerization
chlorides
nucleic acids
RNA
chemistry
lysine
compatibility
magnesium
enzymes
Chlorides
buffers
Nucleic Acids
Allylamine
Catalytic DNA

All Science Journal Classification (ASJC) codes

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

@article{f762d76e03e34095a5f27ffd7e2064a5,
title = "Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates",
abstract = "Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; however, their compatibility with essential RNA World chemistries is unclear. We show that such compartments can enhance key prebiotically-relevant RNA chemistries. We demonstrate that template-directed RNA polymerization is sensitive to polycation identity, with polydiallyldimethylammonium chloride (PDAC) outperforming poly(allylamine), poly(lysine), and poly(arginine) in polycation/RNA coacervates. Differences in RNA diffusion rates between PDAC/RNA and oligoarginine/RNA coacervates imply distinct biophysical environments. Template-directed RNA polymerization is relatively insensitive to Mg 2+ concentration when performed in PDAC/RNA coacervates as compared to buffer, even enabling partial rescue of the reaction in the absence of magnesium. Finally, we show enhanced activities of multiple nucleic acid enzymes including two ribozymes and a deoxyribozyme, underscoring the generality of this approach, in which functional nucleic acids like aptamers and ribozymes, and in some cases key cosolutes localize within the coacervate microenvironments.",
author = "Poudyal, {Raghav R.} and Guth-Metzler, {Rebecca M.} and Veenis, {Andrew J.} and Frankel, {Erica A.} and Keating, {Christine Dolan} and Bevilacqua, {Philip C.}",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41467-019-08353-4",
language = "English (US)",
volume = "10",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates. / Poudyal, Raghav R.; Guth-Metzler, Rebecca M.; Veenis, Andrew J.; Frankel, Erica A.; Keating, Christine Dolan; Bevilacqua, Philip C.

In: Nature communications, Vol. 10, No. 1, 490, 01.12.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates

AU - Poudyal, Raghav R.

AU - Guth-Metzler, Rebecca M.

AU - Veenis, Andrew J.

AU - Frankel, Erica A.

AU - Keating, Christine Dolan

AU - Bevilacqua, Philip C.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; however, their compatibility with essential RNA World chemistries is unclear. We show that such compartments can enhance key prebiotically-relevant RNA chemistries. We demonstrate that template-directed RNA polymerization is sensitive to polycation identity, with polydiallyldimethylammonium chloride (PDAC) outperforming poly(allylamine), poly(lysine), and poly(arginine) in polycation/RNA coacervates. Differences in RNA diffusion rates between PDAC/RNA and oligoarginine/RNA coacervates imply distinct biophysical environments. Template-directed RNA polymerization is relatively insensitive to Mg 2+ concentration when performed in PDAC/RNA coacervates as compared to buffer, even enabling partial rescue of the reaction in the absence of magnesium. Finally, we show enhanced activities of multiple nucleic acid enzymes including two ribozymes and a deoxyribozyme, underscoring the generality of this approach, in which functional nucleic acids like aptamers and ribozymes, and in some cases key cosolutes localize within the coacervate microenvironments.

AB - Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; however, their compatibility with essential RNA World chemistries is unclear. We show that such compartments can enhance key prebiotically-relevant RNA chemistries. We demonstrate that template-directed RNA polymerization is sensitive to polycation identity, with polydiallyldimethylammonium chloride (PDAC) outperforming poly(allylamine), poly(lysine), and poly(arginine) in polycation/RNA coacervates. Differences in RNA diffusion rates between PDAC/RNA and oligoarginine/RNA coacervates imply distinct biophysical environments. Template-directed RNA polymerization is relatively insensitive to Mg 2+ concentration when performed in PDAC/RNA coacervates as compared to buffer, even enabling partial rescue of the reaction in the absence of magnesium. Finally, we show enhanced activities of multiple nucleic acid enzymes including two ribozymes and a deoxyribozyme, underscoring the generality of this approach, in which functional nucleic acids like aptamers and ribozymes, and in some cases key cosolutes localize within the coacervate microenvironments.

UR - http://www.scopus.com/inward/record.url?scp=85060917281&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060917281&partnerID=8YFLogxK

U2 - 10.1038/s41467-019-08353-4

DO - 10.1038/s41467-019-08353-4

M3 - Article

C2 - 30700721

AN - SCOPUS:85060917281

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 490

ER -